Anais da Academia Brasileira de Ciências (2014) 86(2): 867-880 (Annals of the Brazilian Academy of Sciences) Printed version ISSN 0001-3765 / Online version ISSN 1678-2690 http://dx.doi.org/10.1590/0001-3765201420130521 www.scielo.br/aabc Reproductive biology of a bromeligenous frog endemic to the Atlantic Forest: Aparasphenodon arapapa Pimenta, Napoli and Haddad, 2009 (Anura: Hylidae) AMANDA S.F. LANTYER-SILVA1, MIRCO SOLÉ1 and JULIANA ZINA2 1Programa de Pós-Graduação em Ecologia e Conservação da Biodiversidade, Universidade Estadual de Santa Cruz/UESC, Rodovia Jorge Amado, Km 16, 45662-900 Ilhéus, BA, Brasil 2Laboratório de Vertebrados, Departamento de Ciências Biológicas, Universidade Estadual do Sudoeste da Bahia/UESB, Rua José Moreira Sobrinho, Jequiezinho, 45206-190 Jequié, BA, Brasil Manuscript received on December 17, 2013; accepted for publication on March 14, 2014 ABSTRACT The genus Aparasphenodon is restricted to South America and comprises five poorly studied species which present a straight relationship with bromeliads. Herein we present the reproductive biology of the species Aparasphenodon arapapa. Our observations indicate that A. arapapa is a prolonged breeder, reproducing throughout the year using bromeliads as a calling and breeding site. The tadpoles complete their development inside those plants. Males, females and juveniles may also use the bromeliads as a shelter. We also describe the courtship behavior and the parental care of the species with an evidence of temporary fidelity between male and female and propose a new reproductive mode. Key words: reproductive mode, oophagy, parental care, bromeliad. INTRODUCTION of alternative reproductive sites and specialized Although new species of frogs are continually reproductive modes, are still understudied even described, with about more than 100 names being though they could present sets of novel adaptations proposed worldwide each year (Köhler et al. 2005), associated to the taxon occurrence in its habitat in such information on the natural history for this newly a narrow sense, that conservation issues may have to described taxa is seldom provided. Even for taxa take this information into account. One of the factors known for a long time, only recently has information that can be pointed out as a justification for the very become available (e.g. Silva and Juncá 2006, Ruas et few natural history studies of these species is their low al. 2012, Dias et al. 2012). Nevertheless, studies on representativity in anuran communities. Among these natural history are especially important and relevant to anuran breeder specialists are the phytotelm-breeders understand interactions between individuals and their (phyto=plant, telmos=ponds) that depend on water- environment, being useful for conservation action filled plants or plant parts. They exhibit the most plans and phylogenetic studies (Wells 2007, Gomez- complex adaptations to reproduce in these plants (e.g. Mestre et al. 2012). Species exhibiting specialized complex arrangements of parental care, see Gomez- reproduction, including complex courtship, use Mestre et al. 2012). Although comprehension of the evolutionary Correspondence to: Mirco Solé E-mail: [email protected] mechanisms that explain the association between An Acad Bras Cienc (2014) 86 (2) 868 AMANDA S.F. LANTYER-SILVA, MIRCO SOLÉ and JULIANA ZINA frogs and plants has not been fully achieved, a better studies and some ecological and physiological picture has just been acquired (Gomez-Mestre et al. aspects were documented (Mesquita et al. 2004, 2012, Lehtinen et al. 2004, Brown et al. 2010). It Teixeira et al. 2002, Bertoluci et al. 2007, Vilela et is known that phytotelm-breeders had to improve al. 2011). Aparasphenodon arapapa is considered a their adaptations to phytotelmata constraints, such bromelicolous anuran that inhabits only “restinga” as low dissolved oxygen levels, risk of desiccation, areas (Pimenta et al. 2009). The advertisement and unpredictable food availability (Lehtinen et al. call and tadpole of this species have been recently 2004). Additionally, competition may be stronger described (Lourenço-de-Moraes et al. 2013). Herein, intra-specifically (Lehtinen 2004, Lin et al. 2008) we present the habitat use and some reproductive and predation pressure less intense within units of aspects of Aparasphenodon arapapa including phytotelmata when compared to larger water bodies courtship behavior. Because of its specialized and (Kitching 2001). stereotyped behavior in comparison with what is Bromeliads are the most conspicuous known for a large set of anuran species, we also phytotelmata in the coastal regions in Brazil. describe a new reproductive mode for hylid frogs For some anuran species that use bromeliads as in this study, and propose its recognition. microhabitats, adaptations have been observed: small MATERIALS AND METHODS clutch size (e.g. Ranitomeya biolat, von May et al. 2009), endotrophic tadpoles (e.g. Syncope antenori, STUDY AREA Krügel and Richter 1995), oophagy (e.g. Osteopilus Our study was conducted in the Boa União brunneus, Lannoo et al. 1987), cannibalistic larvae Reserve (15°04’S, 39°03’W, 95 m a.s.l.) located (e.g. Ranitomeya ventrimaculata, Summers 1999), in the municipality of Ilhéus, southern Bahia, split clutch (e.g. Scinax perpusillus, Alves-Silva and Brazil. The area is composed by the less known Silva 2009), and parental care (e.g. Dendrobates phytophysignomy of the Atlantic Forest domain, pumilio, Weygoldt 1980). Among bromeliad- called Mussununga Forest, in which vegetational dwellers, some species exhibit morphological traits resemble sandy coastal plains of arboreal adaptations for the use of this microhabitat, such as ‘restingas’ (short trees and sandy soil) (sensu species of the genus Aparasphenodon that present Thomas 2003) (Figure 1). The local climate is a hyper-ossified cranium (Mertens 1950, Pombal tropical wet (Af, according to Köppen 1936); warm 1993, Mesquita et al. 2004), useful for reducing and humid with no defined dry season. water loss by evaporation through phragmotic behavior, a mechanism of sealing the bromeliad with DATA COLLECTION AND DATA ANALYSIS its head (Andrade and Abe 1997). From November 2011 to October 2012, we visited The genus Aparasphenodon comprises five the reserve on a weekly basis (with just a few species (A. arapapa, A. bokermanni, A. brunoi, A. deviations of this frequency of visits). Individuals pomba and A. venezolanus), distributed along the were sampled by visual and auditory search along coastal region of Brazil (Bahia to Santa Catarina) a 300 m long trail. Observations began after sunset and upper Orinoco basin of Venezuela and (approximately 18:00h) and finished with the end Colombia (Mollo Neto and Teixeira 2012, Frost of male vocal activities at about 24:00h. Focal 2014). Only a few studies have addressed aspects animal and all occurrence samplings were adopted of the natural history of species of this genus. for behavioral records (Altmann 1974). Aparasphenodon brunoi and Aparasphenodon Males were recognized by their calling activity bokermanni have been recorded in community or by their position during amplexus, because the An Acad Bras Cienc (2014) 86 (2) REPRODUCTIVE BIOLOGY OF Aparasphenodon arapapa 869 thermohygrometer at least twice during each field trip. We obtained rainfall data from a local station in the nearest municipality Una, about 22 km distant from the study area (except for November, December 2011 and October 2012 which were not considered in the analysis). We carried out statistical analyses using R Core Team for Windows version 2.15.2 (2012) and a significance level of 5% to reject null hypotheses. In order to survey the number of eggs in a clutch, we collected two clutches. Twenty-four eggs were measured (with calipers with 0.01 cm precision) from three different clutches. We Figure 1 - The study area of Aparasphenodon arapapa at the followed the development of tadpoles of A. arapapa municipality of Ilhéus, state of Bahia, Brazil. in one bromeliad and to facilitate observations in field we categorized them using the development vocal sac was undistinguishable. Females were stages of Gosner (1960), into: early (19 to 30), recognized by visual inspection and detection of intermediate (30 to 36) and advanced (37 to 46). oocytes (when gravid) and also by their position Ovarian follicles of two females were observed. during amplexus. We recorded the highest number Two males and two females were collected as of males in calling activity at one point of the trail voucher specimens and deposited in the Zoological at least twice on each field trip, between 18:00h and Collection of Universidade Estadual de Santa Cruz 24:00h. All individuals we found were measured – Herpetological section (adults: MZUESC 11084- (with a caliper of 0.01 cm precision) and weighed 11089/ tadpoles: MZUESC 9097–98; 10354) (with a field scale of 0.1 g precision). We followed under the collection permit provided by Instituto Waichman (1992) for toe-clipping and individuals Chico Mendes de Conservação da Biodiversidade were released at the same site where they were found. (ICMBio) to MS (13708-1). Operational Sex Ratio was the mean of the number RESULTS of females divided by number of males each day (Elmberg 1990). To test the null hypothesis of no ADULTS difference on the snout-vent length (SVL) and body Males of Aparasphenodon arapapa had a mean mass between males and females, we conducted a SVL of 45.4 mm (SD=2 mm; range=41.2-50.2 mm; Mann-Whitney test. Mean occurrence frequency of n=73) and a mean body mass of 3.62g (SD=4.3 g; males and females by night were obtained by dividing range=2.6-4.5 g; n=73); females had a mean SVL of the total number of individuals recorded in the area 53.3 mm (SD=2.4; range=50.0- 60.0 mm; n=23) and along the whole study period by the number of field a mean body mass of 5.5 g (SD=0.75; range=4.0-7.0 trips. To verify whether the mean number of calling g; n=23).